This study analyzed tuberculosis (TB) case data from River Nile State, Sudan between 2011-2013. It found that 15.3% of total reported TB cases were children under 15 years of age. Most cases were newly diagnosed pulmonary TB and occurred in males. Sputum testing confirmed TB in only 15.3% of cases. Treatment success rates were suboptimal at 76.5% for new sputum-positive cases and 88.2% overall. The findings suggest childhood TB is underreported in the region and improved active case detection is needed.

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1 © ???? Journal of Natural Science, Biology and Medicine | Published by Wolters Kluwer - Medknow
Abstract
Introduction: Tuberculosis (TB) is a significant cause of morbidity and mortality among children. The vague symptoms, the
uncertain diagnostic tests and lack of adequate awareness among families all contributed in masking the actual prevalence of
the disease. The objective of this study is to describe the epidemiology of childhood TB in River Nile State (RNS), North Sudan.
Methods: All registered cases of TB aged 15 years and below, at the 13 management units in RNS during 3 years, 2011–2013
were included. The records included epidemiological, clinical, and microbiological data. Results: Of these 1221 total TB notified
cases, children were 187 (15.3%); almost equally distributed across the 3 years of the study period. Males were 56.7%. Most
of the cases (89.9%) were newly diagnosed; among them, pulmonary TB (PTB) constituted 61.5%. Sputum specimen was
tested in 59.4% (111/187) of cases, and only 15.3% (17/111) of specimens were sputum smear positive for new cases. The cure
rate was (76.5%), and the treatment success rate was (88.2%). The death rate was 6.1% among PTB cases and 5.6% among
extra-pulmonary cases. All the 20 (10.7%) children tested for HIV were negative. Conclusion: TB is under-reported in RNS and
treatment outcomes are sub-optimal. Strategies to identify the active case-detection among children are recommended.
Key words: Childhood tuberculosis, River Nile State, Sudan
Department of Pathology, Nile Valley University, Atbara, 1
Department of Peadiatrics and Child
Health, National Ribat University, Khartoum, 2
National Tuberculosis Control Program Coordinator,
River Nile State, Sudan, 3
Department of Medicine, Milton Keynes University Hospital Foundation Trust,
Milton Keynes, Buckinghamshire, UK
Address for correspondence:
Dr. Mohamed H. Ahmed, Department of Medicine, Milton Keynes University Hospital Foundation Trust,
Milton Keynes, Buckinghamshire, UK. E-mail: elziber@yahoo.com
AQ2
all contributed to the resurgence of TB globally.[2]
Indeed,
the highest rates of TB occur in resource-poor countries.[3]
Sudan alone carries 11–15% of the TB burden in the
Eastern Mediterranean Region of the World Health
Organization (WHO).[4]
The estimated incidence of new TB
casesin2010was119/100,000populations,andtheestimated
JNSBM_40_16R3
Original Article
INTRODUCTION
Tuberculosis (TB) is one of the major infections affecting
children worldwide.[1]
It causes significant morbidity and
mortality, especially in infants and young children. However,
accurateinformationontheextentanddistributionof disease
in children is not available for most of the world.[1,2]
Factors
such as overcrowding, poverty, and the HIV epidemic have
Prevalence of tuberculosis among children in
North Sudan: Are we only seeing the tip of the
iceberg?
Wadie M. Elmadhoun,
Elmuntasir Taha1
,
Sufian K. Noor,
Sarra O. Bushara,
Ekhlas O. Ahmed2
,
Hamdan Mustafa2
, Amel
Abdelrahim Sulaiman,
Mohamed H. Ahmed3
AQ4
Access this article online
Quick Response Code:
Website:
www.jnsbm.org
DOI:
**************************
This is an open access article distributed under the terms of the Creative
Commons Attribution-NonCommercial-ShareAlike 3.0 License, which allows
others to remix, tweak, and build upon the work non-commercially, as long as the
author is credited and the new creations are licensed under the identical terms.
For reprints contact: reprints@medknow.com
How to cite this article: We will update details while making issue online***

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Elmadhoun, et al.: Running title missing???AQ1
2Journal of Natural Science, Biology and Medicine | ??? | Vol ? | Issue ?
prevalence was 209/100,000 causing an overall death rate of
24/100,000 annually.[4]
The exact number of deaths among
children is not known, but its important to emphasize that
TB is an important disease affecting child survival.[5]
The natural history and clinical expression of infection of
TB differ substantially in children compared with adults.[6]
It is difficult to confirm the diagnosis of TB by current
microbiological methods. Even in industrialized countries,
the triad of a positive tuberculin skin test, radiographic
and/or clinical manifestations consistent with TB, and
establishing a recent link to a known infectious case of TB
is the “gold standard” for diagnosis.[7]
Further more, poor ascertainment and reporting of cases
of TB prevent accurate estimation of the global burden of
diseaseamongchildren.Whileoverdiagnosisisapossibility,the
majority of cases is not diagnosed, especially where children
with TB can access services only through referral hospitals.[8]
ItisimportanttomentionthatTBinyoungchildrenindicates
recent infection rather than secondary reactivation.[1-8]
The aim of this work was to describe the epidemiology of
TB among children in RNS, North Sudan; we believe that, in
low-resource settings, such as our country, epidemiological
data can be used to monitor TB transmission in the
community and to evaluate the effectiveness of the
National TB Control programme.
METHODS
Settings
River Nile State (RNS) lies in North Sudan, (32–36° N
and 16–22° E), covering an area of 124,000 km2
, and the
population is about 1,250,000 composed of different ethnic
groups. The most important cities are Ed Damer, Atbara,
Shendi, Berber and Abu Hamad. There are seven working
TB Management Units (TBMUs), integrated within the
general health system and distributed over the seven
localities of the state, staffed with medical and nursing
personnel, and social workers. TBMUs are the institutions
where suspected TB patients are diagnosed and treated.
Data collection tools
Data were collected from the TB records, at the TBMUs.
The records included the following epidemiological,
clinical, and microbiological data: Name, age, sex, residence,
centre of diagnosis and management, referral source, date
of presentation, site of the disease, signs and symptoms
with duration, whether new or re-treatment case, sputum
microscopy tests initially and periodically, other diagnostic
methods, treatment category, time of sputum conversion,
treatment outcomes, and HIV status. In RNS, TB is
diagnosed using a combination of a patient history, physical
examination, and diagnostic tests, including sputum
microscopy, chest X-ray, and tissue samples.
Data analysis
Adescriptiveanalysisfortheselectedvariableswasperformed
using SPSS computer program version 20.0. The frequency
distribution of the different variables and the percentages of
cases with data on these variables was calculated. Age was
characterized by mean and standard deviation. P < 0.05 was
consideredstatisticallysignificantforcomparingproportions.
Ethical issues
EthicalapprovalwasobtainedfortheEthicalCommitteeof the
Facultyof MedicineandHealthSciences,NileValleyUniversity.
RESULTS
During the 3-year period of study, 187 children (15 years
and below) were registered in the records of the TB control
program in RNS, out of the 1221 total cases during the same
period, representing (15.3%). Almost equal number of cases
were diagnosed every year, 62, 60, 65 in the years 2011, 2012,
and 2013, respectively. This distribution gives a rough case
notification rate of 5/100000 population. Males constituted
56.7% with a male to female ratio of 1.3:1. Seven TMBUs
cases were diagnosed. However, most cases in this study,
53.5% (100/187) were diagnosed in Atbara center [Table 1].
Concerning the type of patients at the start of treatment,
89.9% (168/187) were new TB cases, 3.2% (6/187) were
relapses, and only one case (0.5%) was a defaulter [Table 2].
AQ3
Table 1: Sociodemographic characteristics of
registered children with tuberculosis in River
Nile State, Sudan 2011-2013 (n=187)
Characteristic Variable n Percentage
Sex Male 106 56.7
Female 81 43.3
Age group
(years)
<1 13 7.0
1-2 42 22.5
>2-<5 32 17.1
5-10 53 28.3
>10 47 25.1
Residence by
locality
Atbara 37 19.8
Eldamer 62 33.2
Berber 46 24.6
Shendi 33 17.6
Abu Hamad 9 4.8
TBMU center Atbara Teaching Hospital 100 53.5
Eldamar Hospital 14 7.5
Berber Hospital 29 15.5
Abu Hamad Hospital 6 3.2
Kaboushia Hospital 3 1.6
Alketyab Hospital 4 2.1
Shendi Hospital 31 16.6
TBMU:Tuberculosis management unit

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Elmadhoun, et al.: Running title missing???AQ1
3 Journal of Natural Science, Biology and Medicine | ??? | Vol ? | Issue ?
Pulmonary TB (PTB) cases were 61.5% (115/187) and
extra-pulmonary cases were 38.5% (72/187).
The total number of children tested for sputum were 59.4%
(111/187); among them, only 15.3% (17/111) were sputum
smear-positive new cases and 84.7% (94/111) were new
sputum smear-negative cases.
The treatment outcome for children was displayed in
Table3.However,duetothelimitednumberof newsputum
smear-positive cases, all indicators of the control program
were sub-optimal. When considering the WHO indicators
for the assessment of the control program outcomes
that takes into account only new sputum smear-positive
cases as a denominator; the cure rate was (76.5%), and
the treatment success rate was (88.2%). For comparison,
when considering the whole cohort of PTB cases, the cure
rate was 12.2%, and treatment completion rate was 63.5%.
The death rate was 6.1% among PTB cases and 5.6%
among extra-pulmonary cases [Table 3]. All 20 (10.7%)
children tested for HIV were negative.
DISCUSSION
TB is one of the greatest challenges for all health
authorities across the globe. In this study, among the
1221 total cases of TB reported in RNS, children were
187 (15.3%). It is to be mentioned that globally, the
WHO estimated the prevalence of childhood TB is
around 6% of total cases.[9]
Our finding is higher than
the reported global burden of TB in children. For
instance, among the 4,452,860 new cases reported in
2010 by the 22 countries with the highest burden of TB,
only 157,135, (3.5%) (range, 0.1–15.0%), of the cases
were children. There is general agreement in literature
that the best estimates suggest that children account
for approximately 11% of the burden of disease from
TB.[1,7]
In addition, it is estimated that only 50% of cases
of childhood TB was notified to the National Control
programmes. This low notification rate was attributed
to many factors, including the nonspecific symptoms
in children, the uncertain diagnosis, poor accessibility
to health facilities, poverty, and unawareness among
families.[10]
It is plausible to suggest that these same
factors are also contributing to the high incidence
of childhood TB expected in Sudan and to the low
reporting rate as well.
To overcome this obstacle, the WHO launched the
“roadmap for childhood TB” to improve case-detection,
diagnosis, and treatment outcome, and also advocates
for better commitment and accountability at all levels of
the health system and the community.[11]
In this context,
active case finding activities of proven yield included:
Household contact screening, private-public mix services,
Table 2: The clinical characteristics of children
with tuberculosis in River Nile State, Sudan
2011-2013 (n=187)
Characteristic Variable n Percentage
Type of patient at start
of treatment
New TB case 168 89.8
Relapse 6 3.2
Transferred 3 1.6
Defaulter 1 0.5
Other types* 9 4.8
Site of TB involvement Pulmonary 115 61.5
Extra-pulmonary 72 38.5
Sputum positive for
AFB (for PTB cases)
23 12.3
Symptom Cough 102 54.5
Fever and sweating 115 61.5
Chest pain 1 0.5
Loss of weight 26 13.9
Diarrhea 18 9.6
Lymphadenopathy 21 11.2
Cold abscess 3 1.6
Other symptoms+
23 12.3
Duration of symptoms <1 week 7 3.7
2 weeks 19 10.2
3 weeks 16 8.6
1 month 57 30.5
6 weeks 11 5.9
2 months 40 21.4
3 months 21 11.2
1 year 8 4.3
>1 year 8 4.3
*Other types include: (1) Symptomatic cases, sputum negative, has been previously
treated;(2)patientsnotknowntreatedorunknownoutcome,orreturnedtotreatment
from PTB negative or extra-pulmonary TB, +
Other symptoms include: Discharging
sinus,abdominalpaingeneralill-health,etc.,AFB:AcidfastBacilli,PTB:PulmonaryTB,
TB:Tuberculosis
Table 3: Treatment outcome of children with
tuberculosis in River Nile State, Sudan 2011-2013
(n=187)
Characteristic Variable n Percentage
Treatment outcome for
the new smear-positive
pulmonary TB cases
(n=17) based on WHO
criteria
Cure 13 76.5
Completed treatment 2 11.8
Treatment success rate 15 88.2
Default 1 5.9
Transferred 1 5.9
Treatment outcome for
the whole study group
of TB cases (n=187)
Pulmonary TB
cases (n=115)
Cure 14 12.2
Completed treatment 73 63.5
Died 7 6.1
Default 17 14.8
Transferred 4 3.5
Extra-pulmonary TB
cases (n=72)
Cure 0 0
Completed treatment 54 75
Died 4 5.6
Default 7 9.7
Transferred 7 9.7
TB:Tuberculosis,WHO:World Health Organization

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Elmadhoun, et al.: Running title missing???AQ1
4Journal of Natural Science, Biology and Medicine | ??? | Vol ? | Issue ?
mobile health chest maps, community home-based care
visits, and screening of children at school in addition to
safe motherhood health services.[10]
It is to be mentioned that age per se has an important impact
in the natural history of disease progression. For instance,
in our study, children < 2 years were minority (7.6%) when
compared to those more than 5 years (45%). This finding
has been attributed to the natural history of TB in children
which differs substantially in the two age groups.[12]
Primary
infection before 2 years of age frequently progresses
to serious disease within the first 12 months without
significant prior symptoms. Whereas primary infection
between 2 and 10 years of age rarely progresses to
serious disease, and such progression was associated with
significant clinical symptoms. In children aged more than
3 years, the presence of symptoms represented a high
chance to establish a clinical diagnosis before serious
disease progression. Primary infection after 10 years of
age frequently progresses to adult-type disease.[13]
In this study, cough was reported in 54.5% while fever and
sweating were reported in 61.5%. It has been stated that
with airway involvement, the usual presenting symptom is
a persistent, nonremitting cough that is unresponsive to
the treatment for the likely alternative causes.[13]
Clinical
signs are often subtle, and no diagnostic scoring system
has been adequately verified.[14]
The duration of symptoms varies, but most cases (96.3%)
run a chronic coarse (more than 2 weeks) before establishing
diagnosis while only (3.7%) were diagnosed within 1 week
duration. This delay could be explained by the natural
history of TB and both the variations in susceptibility to
disease and the diverse spectrum of clinical manifestations
observed in children due to the sequence of events that
follows primary infection with Mycobacterium tuberculosis.[13]
Microscopical examination of sputum for bacteriologic
confirmation was only used in (27.3%) of the studied
children; this could be due to the difficulty of collecting
spontaneously produced sputum in children. In addition,
a gastric aspiration that needs training, and hospital
setting was not feasible at the diagnostic centers in our
settings. DOTS/STOP TB strategies have been effective
epidemiological tools in targeting sputum smear-positive
cases in adults. However, children deemed to be ignored
as they are unable to produce sputum. Therefore,
children contribute very little to transmission within
communities.[15-17]
Chest radiography was used in 44.9% of cases as X-ray has
always been highly suggestive of a diagnosis of PTB but it
depends on technical quality and facilities which are major
challenges in developing countries. Another investigation
used in the studied children was fine-needle aspiration
biopsy, which was used in (5.9%). This technique was
proven useful in children with a peripheral lymph-node
mass.[18,19]
In our study, we identified PTB in 61.5% of the cases while
the remaining 38.5% were extra-PTB. This percentage
is less than that reported in South Africa, 76.7% for
pulmonary and 25% for extra-thoracic TB while in the
USA 73.6% was PTB and 18.7% were extra-PTB.[20,21]
These variations may be attributed to disease prevalence as
well as the availability of methods of early diagnosis and
early notification. Furthermore, many studies highlighted
the difficulty in confirmation of the disease in children
that resulted in poor reporting, especially in endemic
areas with limited resources.[22,23]
This poor reporting has
been identified as a major factor contributing to the poor
treatment indicators.[8]
The outcome of treatment in this study was generally
sub-optimal. For the new smear-positive pulmonary cases,
the cure rate and treatment completion rate were 76.5%
and 88.2% respectively. However, due to the scarcity
of new smear-positive cases among children, we also
calculated the treatment outcome for the whole cohort,
i.e., all cases underwent sputum testing as a denominator
and not only the new cases. By doing so, the cure rate
and treatment completion rate dropped to 12.2% and
63.5%, respectively.
Despite the fact that children with TB respond well
to and tolerate the same basic treatment regimens as
used for adults,[7]
the situation is sub-optimal in our
settings. This was evidenced by the fewer number of
children achieving required treatment targets. Here, poor
compliance with treatment may constitute a contributing
factor.
This study has some limitations. The cross-sectional
design may reflect only temporal associations. In addition,
a health facility-based study is another limitation that
may not allow generalizations to be made about the
exact situation in the community. However, with the
limited resources in our setting, other alternative ways
to survey the community are not feasible. It is possible
to consider the small sample size as one limitation of
this study; however, this was the total number of cases
notified to the control program during study period.
It is well reported in literature that diagnosis of TB in
children is an ambiguous area[15,23]
in addition to problems
of data recording in TB registries at TBMUs. Despite
these limitations, we assume that this study is the first
of its kind in Sudan, reflecting the epidemiology of

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Elmadhoun, et al.: Running title missing???AQ1
5 Journal of Natural Science, Biology and Medicine | ??? | Vol ? | Issue ?
childhood TB with special emphasis on the assessment
indicators of the control program of DOTS/STOP TB
strategies. We recommend further studies to explore the
whole picture in our country, hopefully, using “intensified
case-detection” strategies.
CONCLUSION
The epidemiology of childhood TB in RNS as in many
other developing countries is masked by many factors that
result is low case-detection rate, poor ascertainment of
diagnosis, and sub-optimal treatment outcome.
Acknowledgment
we are thankful to the Swiss Embassy for financing this
work. Our thanks are extended to the administrators and
statisticians at the State Ministry of Health, RNS for their
collaboration.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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